Providing descriptive data on parasite diversity and load in sister species is a first step in addressing the role of host-parasite coevolution in the speciation process. In this study we compare the parasite faunas of the closely related hedgehog species Erinaceus europaeus and E. roumanicus from the Czech Republic where both occur in limited sympatry. We examined 109 hedgehogs from 21 localities within this secondary contact zone. Three species of ectoparasites and nine species of endoparasites were recorded. Significantly higher abundances and prevalences were found for Capillaria spp. and Brachylaemus erinacei in E. europaeus compared to E. roumanicus and higher mean infection rates and prevalences for Hymenolepis erinacei, Physaloptera clausa and Nephridiorhynchus major in E. roumanicus compared to E. europaeus. Divergence in the composition of the parasite fauna, except for Capillaria spp., which seem to be very unspecific, may be related to the complicated demography of their hosts connected with Pleistocene climate oscillations and consequent range dynamics. The fact that all parasite species with different abundances in E. europaeus and E. roumanicus belong to intestinal forms indicates a possible diversification of trophic niches between both sister hedgehog species.
Citation: Pfäffle M, Černá Bolfíková B, Hulva P, Petney T (2014) Different Parasite Faunas in Sympatric Populations of Sister Hedgehog Species in a Secondary Contact Zone. PLoS ONE 9(12): e114030. https://doi.org/10.1371/journal.pone.0114030
Editor: Helge Thorsten Lumbsch, Field Museum of Natural History, United States of America
Received: August 7, 2014; Accepted: November 3, 2014; Published: December 3, 2014
Copyright: © 2014 Pfäffle et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.
Funding: The work was supported by Institutional Research Support grant No. SVV-2013-267 201 and GAUK 702214 (BCB PH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
The restriction of populations of a wide variety of European species to spatially limited refuge areas during the cyclic climatic changes of the Pleistocene, together with the associated genetic bottleneck, has had a great impact on the genetic characteristics of the species and on speciation . Many of the vertebrate species so affected harbor a specific parasite community which undergoes the same cyclic population, spatial and genetic restrictions, potentially leading to community changes, loss of genetic diversity and speciation , .
Hedgehogs were repeatedly restricted to glacial refuges during ice age maxima with subsequent re-colonization of Europe , . Recent Western European hedgehogs (Erinaceus europaeus, EE) had a disjunct distribution on the Iberian Peninsula and Italy (Apennine and Sicilian refuges), while the northern white-breasted hedgehog (E. roumanicus, ER) survived in the Balkan refuge and the southern white-breasted hedgehog (E. concolor, EC) was found in the Middle East, separated from ER by the Bosporus and the Caucasus Mountains , .
Until recently ER was considered to belong either to EE or to EC and it has only recently been defined as a valid species . Studies based on mitochondrial and nuclear sequence data suggest the sister position of ER and EC with a divergence time of approximately 1–2 Myr, , , . Bannikova et al.  also showed the sister status of EE and Erinaceus amurensis (EA) with the time of separation being estimated as approximately 1 Myr. These two groups – EE + EA and ER + EC probably split during the Pliocene . The secondary contact between ER and EE in central Europe probably originated after the last ice age during the Neolithic deforestation . The distribution of these species is parapatric, however, the zone of overlap in central Europe reaches its greatest within the Czech Republic , . Until now, no interspecific hybridization in the area of Central Europe has been recorded , , although Bogdanov et al.  reported a possible hybrid individual from Russia where the contact zone is younger.
Currently, the Western Palearctic is inhabited by all three hedgehog species. EC ranges from Asia Minor to Israel, Syria, Lebanon, Iraq and Iran; and the southern Caucasus . ER has a distribution extending from Central and Eastern Europe, the Baltic and the Balkan Peninsula, the Greek Adriatic including Rhodes and eastwards through Belarus, the Ukraine, and Russia, reaching as far as the Ob River in Siberia. In the south, its range extends as far as the northern Caucasus and the island of Crete. Within the Mediterranean region, it ranges from Italy and Slovenia, through the Balkan Peninsula, extending south into Thracian (i.e. European) Turkey . These two species are separated in the Caucasus Mountains, but information about a contact zone is missing. The distribution of EE extends from the British Isles and the Iberian peninsula, westwards through much of western to central Europe; and from southern Fennoscandia, and the northern Baltic to north-west Russia. In the Mediterranean, it occurs in Portugal, France (including Corsica), Spain and Italy including Sardinia and Sicily . In central Europe and in Russia and Estonia, the range of EE overlaps with that of ER. Figure 1 shows the distribution of EE and ER as well as their contact zones in the western Palearctic.
Size of circles represents the number of hedgehogs from the different locations (modified after ).
Hedgehogs host a wide variety of different macroparasites, endoparasitic helminths and ectoparasitic ticks, fleas and mites , with many widely distributed species but also some species which are narrowly endemic, such as Brachylecithum mackoi from the island of Elba . These may play an important role in host morbidity and mortality (see e.g. , ). However, very little is known about the similarities and differences in the parasite fauna of the three Eurasian hedgehog species. Given the relatively deep split defining these hedgehog species, as well as the cyclic restriction in distributional area and population size, we predict that parasite co-speciation may have occurred and that the parasite community infesting the particular host species may differ. Thus, investigating the composition of the parasite fauna may provide valuable information regarding the phylogenetic differentiation, niche and population dynamics, diversification and species interactions in this group.
In this study we compare the parasite faunas of ER and EE from contact zones in the Czech Republic and interpret this information with regard to the phylogeography of the genus.
Material and Methods
The hedgehogs from this study were either provided by wildlife rescue centers, where the animals died naturally, or were collected as road kills. Therefore an ethical approval by the relevant ethics committee was not required. All specimens were frozen at −20°C until they were used for dissection. Prior to examination individuals were thawed at room temperature, weighed and the sex was determined. Animals were classified either as hoglets (<100 g), juveniles (<500 g) or adults (>500 g) .
The samples originated from 21 different areas in the Czech Republic (Figure 1, Table S1). Collections were made during 2008–2011. In total we examined 109 animals (ER = 27, EE = 82). For ER we collected 19 juveniles (female = 11, male = 8) and seven adults (female = 2, male = 5). For EE we found eight hoglets (female = 3, male = 5), 61 juveniles (female = 30, male = 31) and 12 adults (female = 5, male = 7). Genetic analysis of mitochondrial DNA and nucelar microsatellites were used for determination of 20 specimens of EE and 14 specimens of ER, which were identical with the study of Bolfíková & Hulva . Considering the presumed absence of hybridization (or very low degree of introgression) between both species in Central Europe ascertained by reciprocal monophyly of respective clades and the absence of intermediate phenotypes in the analysis of more than 200 individuals within the contact zone , morphology-based discrimination was used for remaining specimens within the present study.
Fleas and ticks were collected, identified to life history stage, sex (if not immature) as well as to species after Beaucournou & Launay  and Arthur , respectively, and subsequently quantified. Due to the difficulty of quantifying infestation rates, mites were not included in the examination. The body cavity (peritoneum), connective tissue and the surface of the organs were examined for encysted acanthocephalans. The lung was examined under a binocular microscope (Stemi 2000, Carl Zeiss Mikroskopie, Jena, 07740, Germany) for nematode infections. Crenosoma striatum and Capillaria aerophila from the bronchi and bronchioles were quantified. The stomach and the intestine were stored overnight in tap water in the refrigerator at 4°C to allow the intestinal parasites from the intestinal wall to move into the water. The next day, the water and the intestinal sections were examined under a binocular microscope (water with transmitted light, intestinal sections with direct light). All parasites found were identified to species after Beck & Pantchev  and quantified. Information about the taxonomic status, the habitat preference and the host specificity of the parasites found in this study are listed in Table S2.
All statistical analyses were conducted using IBM SPSS Statistics Version 20. To test for differences in parasite abundance between sex, age and species groups, a Mann-Whitney U-test was used. To test for differences in parasite prevalence between sex, age and species group we used a chi-square test.
In total, twelve parasite species were determined (Table 1). Ectoparasites included one flea species, the hedgehog flea Archaeopsylla erinacei and two tick species, the hedgehog tick Ixodes hexagonus and the castor bean tick I. ricinus. The lungworm C. striatum and C. aerophila were found in the lungs. In the intestines Capillaria spp., Physaloptera clausa (only found in the stomach) and one unidentified nematode, the trematode Brachylaemus erinacei, the cestode Hymenolepis erinacei and the acanthocephalans Nephridiorhynchus major and Plagiorhynchus cylindraceus were found.
Since none of the hoglets were parasitized, they were eliminated from further statistical analysis. We did not find any significant differences in parasitization between the sexes. We therefore pooled the sexes in each age group. We could not find any differences between age groups for ER. For EE we found higher mean abundances of C. striatum (p = 0.01), B. erinacei (p = 0.006) and lower abundances of H. erinacei (p = 0.02) in juveniles compared to adult animals (Table 1). Therefore we treated hedgehog age groups for those parasites separately for further statistical analysis. For all other parasites the age groups were pooled.
When we compared the differences in mean parasite infection rates between the two hedgehog species (Mann-Whitney U-test) we found significant differences for H. erinacei from the intestines for juveniles (p = 0.009), B. erinacei for juveniles (p<0.001), Capillaria spp. (p = 0.026), P. clausa (p<0.001) and N. major (p<0.001). The infection rates with B. erinacei and Capillaria spp. were higher in EE, while ER showed higher infection rates with H. erinacei, P. clausa and N. major (Table 1). Similar results were found when we compared the prevalences of the parasite species between EE and ER. EE showed higher prevalences of B. erinacei in juveniles (χ21 = 13.015, p<0.001), while ER had higher prevalences for P. clausa (χ21 = 20.371, p<0.001) and N. major (χ21 = 20.53, p<0.001).
Neutral and adaptive changes during parasite-host coevolution are likely to affect the population and community attributes in both the host and the parasite. In the host species, with demography and range history affected by Pleistocene climatic oscillations, parasites may undergo complicated evolution . Neutral evolution might occur during refugial, peripatric isolation and recurrent bottlenecks during population re-expansions, including founder effects causing parasite release, genetic drift and other factors acting on small populations. Site-specific adaptive responses may occur as well. These may culminate in the extinction of particular parasite species in a particular host lineage or in allopatric speciation. Both would contribute to divergence of parasite faunas between sister host species. On the other hand, parasites may affect evolution of the host, for example via parasite-mediated selection acting in genes regulating immune defense, and may contribute to the host speciation process. Here we show that although there do not appear to be any major morphological changes in the species infesting the two hedgehog species in their zone of overlap, there are considerable differences in the prevalence and intensity of infestation by a variety of endoparasitic species. In order to determine how significant these changes are it is also necessary to consider completely allopatric population of both host species.
Divergent patterns of parasite diversity and load
Many studies on the parasite fauna of E. erinacei were carried out in the late 1970s and 1980s (e.g. –). These are complimented by several more recent studies , –. In contrast to this, only limited information is available on the parasites of EC (e.g. ) and ER (e.g. ). With the exception of the work of  using fecal analysis to determine the helminth fauna of EE and ER in the contact zone in Poland, comparative studies for both species are lacking.
All parasites found in this study have been found previously in or on hedgehogs (e.g. , , , –), although molecular analysis will be needed to confirm that no sibling species are present. If available, when comparing this study to other studies hedgehog sample size (n) and mean abundances () of the other studies will be provided in brackets.
Abundances and prevalences of the flea A. erinacei from this study are relatively low. Egli  reports prevalences from EE (n = 135) of 43.7% in Switzerland and Visser et al.  of 84.2% in Germany (n = 76). This also applies for ER from Hungary where Földvari et al.  found prevalences between 26.3% and 72.1% (n = 247). Beck & Clark  and Beck et al.  even state that every hedgehog is to a greater or lesser extent infested with the hedgehog flea.
Both I. ricinus and I. hexagonus are also frequently found on hedgehogs. As for the hedgehog flea, tick abundances and prevalence were lower in the present study compared to others. Ixodes ricinus prevalences on hedgehogs from Germany (23.4%, n = 133, = 2.83 ) and Switzerland (11.1%, n = 135, ) were higher than 0% for EE and 4% for ER in the present study. For I. hexagonus Pfäffle  found prevalences of 53.3% (n = 133, = 47.56) and 40% (n = 30, = 23.77) for EE from Germany and the UK, respectively. Egli  determined I. hexagonus prevalences of 58.5% for EE (n = 135). However, Földvari et al.  found I. hexagonus prevalences of only 1.1% on ER from Hungary (n = 247). They indicate that this low prevalence could be related to the high hedgehog density on Margaret Island where the study was conducted. Such high hedgehog population densities in semi-natural environments might lead to higher densities of I. ricinus compared to I. hexagonus . Almost all of the animals from the present study came from wildlife rescue centers where they were treated for injuries or symptoms of disease. During this time both ticks and fleas might have been collected by the caretakers or left and dropped of the host, respectively. Therefore our data for ectoparasite prevalences and abundances might well be imprecise and not express the natural infestation rates of EE and ER in the Czech Republic. However, the results do provide an insight into the species of ectoparasites found on both Czech hedgehog species.
The lungworm C. striatum is specific to hedgehogs and the most important parasite of the lung , . Depending on the habitat and the type of examination carried out (coprological vs. dissection), prevalences lie between 45% and 77.5% for EE ( dissection, n = 133, 66.4%, = 20.88;  coprological, n = 127, 52–72.3%;  dissection, n = 53, 66%;  dissection, n = 125, 62.4%, = 46.1;  coprological, n = 155, 77.5%). This is comparable with the results of the present study (25–56.7%, = 1.18–17.83). It seems that infection rates of C. striatum in ER are typically lower than in EE. Furmaga  found prevalences of 14.29% (dissection, n = 14) and Mizgajska et al.  found prevalences of 4.6% (coprological, n = 44). In the present study no significant differences between the infection rates of C. striatum of EE and ER were found and the intensity of infections probably do not depend on the hedgehog species but on the distribution of infected intermediate hosts (land snails), individual food preferences and immune status.
Capillaria aerophila is found in the smaller bronchi and is usually less abundant than the lungworm C. striatum, but can cause similar symptoms, such as weight loss, bronchitis and pulmonary damage , , . The prevalences of C. aerophila found in EE from the present study are comparable to findings from other locations (Table 2). The prevalence of C. aerophila infections in ER is comparably lower than the prevalences found in the study of Mizgajska et al. . However, it should be noted that the information about the parasite fauna of ER is very scarce.
In addition to the findings from Edelenyi & Szabo , this is the first time that P. cylindraceus has been described for ER, although it has been described from the Czech Republic in EE by Prokopic  (1957, syn. Prosthorhynchus jormosus). It is an intestinal parasite of passerine birds which is sporadically found in the intestinal tracts of mammals, causing diarrhea, peritonitis and sometimes increased mortality . Infections seem to occur more often in juveniles than in adult animals, since younger animals also feed on unpalatable prey like woodlice, which are the intermediate hosts for this parasite , . However, we were not able to find significant differences in infection rates between adults and juveniles neither for EE nor for ER.
Cestode infections are rare for EE, prevalence is normally low and restricted to certain regions (e.g.  EE, n = 754, 0.39%;  EE, n = 39, 8%;  EE, n = 437, 0.7%). In ER and EC infections seem to be more common ( EC, n = 18, 55%; Pfäffle unpublished data). However, in the present study only one EE and three ER were infected with H. erinacei, while Mizgajska et al.  did not find any cestode infections at all. All three infected ER came from Prague, while the infected EE originated from Kocbere. These results indicate that the abundance of H. erinacei might also be restricted to certain regions in the Czech Republic. Nevertheless, the sample size might have been too small to support this hypothesis and it is not possible to draw conclusions as to whether the differences in infection rates are species dependent on or are influenced by other factors.
We found higher abundances and prevalences of B. erinacei in juvenile EE compared to juvenile ER and higher mean infection rates with Capillaria spp. in EE compared to ER in all age groups. Abundances and prevalence of P. clausa and N. major where higher in ER compared to EE (all age groups). Capillaria spp. are common parasites of hedgehogs and can reach high prevalence (up to 90%) and intensities (see , , ). Capillaria spp. can be transmitted directly or indirectly via the ingestion of earthworms. They can have a severe effect on the body condition of hedgehogs, which might be increased during periods of high stress, for example during the reproductive phase or hibernation, and higher hedgehog population densities might increase the transmission rates between individuals, hence increasing prevalences and abundances . The work of Mizgajska et al.  on Capillaria spp. showed infections in EE and ER which were the opposite of those found in the present study, with ER having higher prevalences than EE. It seems that this parasite is neither specific for, nor occurs predominantly in, a certain hedgehog species and that there is a high variability in infection rates dependent on region and habitat.
Brachylaemus infections were both higher in prevalence and abundance in juvenile EE than in juvenile ER. This is comparable to the study by Mizgajska et al. , where only EE (n = 15, 33%) were infected with trematodes. Brachylaemus erinacei is host specific , transmitted via the ingestion of various intermediate gastropod hosts  and can cause diarrhea, hemorrhagic enteritis, inflammation of the bile ducts, anemia and death , , .
Both P. clausa and N. major are uncommon in EE but occur in both Eastern European hedgehog species ( EC, n = 41, P. clausa: 72.2%, N. major: 50%;  ER, n = 44, P. clausa: 13.6%;  ER, n = 14, P. clausa: 28.57, N. major: 7.14%;  EC, n = 11, N. major: 63.64%). Studies from southern Europe also found those parasites in EE ( Iberian Peninsula, Spain, n = 125, P. clausa: 6.4%, N. major: 0.8%;  Sicily, Italy, n = 39, N. major: 69.2%;  Sicily, Sardinia, Emilia-Romagna, Italy, n = 34–53, P. clausa: 0–3%, N. major: 0–69%). However, more recent studies did not find either of these species in EE from Central Europe and the UK , , . Both parasite species are transmitted via the ingestion of infected insect intermediate hosts .
In general, the parasite fauna of the best studied species, EE, is relatively consistent throughout its range, although data from Spain ,  and Italy , ,  suggest that at least within these refuges there is a slightly higher parasite species diversity than further north (Table 2).
A detailed comparison of the ecology of host both species is still missing. The existence of a relatively large zone of overlap can be viewed as a natural, large scale, common-garden experiment, which could be utilized for studying the ecological diversification of both lineages with a similar environmental background. The landscape genetic analysis from central Europe points to differences in the altitudinal distribution of EE and ER, indicating at least some ecological differentiation . However, both species can occur in similar habitats and even syntopically, in rural, suburban and urban habitats. EE and ER seem to be essentially similar in their feeding ecology (e.g. –). The diet consists mainly of a variety of invertebrates, usually with a few main prey types such as beetles, caterpillars, earthworms, slugs and snails, which can act as intermediate hosts of various parasite species . However animals from different regions show their own particular spectrum of prey items . The fact that all parasite species with significantly different abundances in EE and ER are intestinal forms nevertheless indicates possible diversification of trophic niches between these sister hedgehog species.
Although definite quantitative differences were found in prevalences and intensities of infection by certain parasite species between the two hedgehog species, qualitative differences in terms of differences in species composition were not apparent. However, as species identification was carried out morphologically, this does not exclude the possibility of cryptic variation in studied species. In order to determine the degree of divergence, and potentially introgression after secondary contact, a molecular study of the parasites should be carried out.
Origins from dissected hedgehog from the Czech Republic.
Taxonomic status, niche and host specificity of parasites found in the present study.
We would like to thank the wildlife rescue centers in Benesov, Bruntal, Jaromer, Prague, Tachov, Vlasim and Zdena Dvorska for providing us with hedgehogs and Dr. Jasmin Skuballa, Dominic Stoll and André Gensch for help with the examinations of the animals and analyzing of the data.
Conceived and designed the experiments: MP BCB PH TP. Performed the experiments: MP. Analyzed the data: MP TP. Contributed reagents/materials/analysis tools: BCB PH. Wrote the paper: MP BCB PH TP.
- 1. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913.
- 2. Nieberding CM, Durette-Desset M-C, Vanderpoorten A, Casanova JC, Ribas A, et al. (2008) Geography and host biogeography matter for understanding the phylogeography of a parasite. Mol Phylogenet Evol 47:538–554.
- 3. Criscione CD (2008) Parasite co-structure: broad and local scale approaches. Parasite 15:439–443.
- 4. Santucci F, Emerson BC, Hewitt GM (1998) Mitochondrial DNA phylogeography of European hedgehogs. Mol Ecol 7:1163–1172.
- 5. Seddon JM, Santucci F, Reeve NJ, Hewitt GM (2002) Caucasus Mountains divide postulated postglacial colonization routes in the white-breasted hedgehog, Erinaceus concolor. J Evol Biol 15:463–467.
- 6. Sommer RS (2007) When east meets west: the sub-fossil footprints of the west European hedgehog and the northern white-breasted hedgehog during the Late Quaternary in Europe. J Zool 273:82–89.
- 7. Hutterer R (2005) Order Erinaceomorpha, In: Wilson DE, Reeder DM, editors. Mammal Species of the World, 3rd Edition Baltimore: JHU Press. Pp.212–219.
- 8. Seddon JM, Santucci F, Reeve NJ, Hewitt GM (2001) DNA footprints of European hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene refugia, postglacial expansion and colonization routes. Mol Ecol 10:2187–2198.
- 9. Bannikova AA, Lebedev VS, Abramov AV, Rozhnov VV (2014) Contrasting evolutionary history of hedgehogs and gymnures (Mammalia: Erinaceomorpha) as inferred from a multigene study. Biol J Linnean Soc 112:499–519.
- 10. Bolfíková B, Hulva P (2012) Microevolution of sympatry: landscape genetics of hedgehogs Erinaceus europaeus and E. roumanicus in Central Europe. Heredity 108:248–255.
- 11. Andera M (2010) Current distributional status of insectivores in the Czech Republic (Eulipotyphla). Lynx (Praha) 41:15–63.
- 12. Bogdanov AS, Bannikova AA, Pirusskii YM, Formozov NA (2009) The first genetic evidence of hybridization between west European and northern white-breasted hedgehogs (Erinaceus europaeus and E. roumanicus) in Moscow Region. Biol Bull 36:647–651.
- 13. Reeve N (1994) Hedgehogs. London: T & AD Poyser (Natural History).
- 14. Casanova JC, Ribas A (2004) Description of Brachylecithum mackoi n. sp. (Digenea: Dicrocoeliidae) from the European hedgehog, Erinaceus europaeus (Insectivora: Erinaceidae). J Parasitol 90:793–796.
- 15. Pfäffle M, Petney T, Elgas M, Skuballa J, Taraschewski H (2009) Tick-induced blood loss leads to regenerative anaemia in the European hedgehog (Erinaceus europaeus). Parasitology 136:443–452.
- 16. Pfäffle M (2010) Influence of parasites on fitness parameters of the European hedgehog (Erinaceus europaeus). PhD thesis, Karlsruhe Institute of Technology (KIT). Available: http://d-nb.info/100808445X/34. Accessed 7 August 2014.
- 17. Beaucournou JC, Launay H (1990) Faune de France Vol. 76: Les puces (Siphonaptera) de France et du Bassin Méditerranéen Occidental. Paris: Fédération Française des Sociétés de Sciences Naturelles.
- 18. Arthur DR (1963) British ticks. London: Butterworths.
- 19. Beck W, Pantchev N (2012) Praktische Parasitologie bei Heimtieren: Kleinsäuger – Vögel – Reptilien – Bienen. Hannover: Schlütersche Verlagsgesellschaft.
- 20. Hoberg EP (1995) Historical biogeography and modes of speciation across high-latitude seas of the Holarctic: concepts for host – parasite coevolution among the Phocini (Phocidae) and Tetrabothriidae (Eucestoda). Can J Zool 73:45–57.
- 21. Timme A (1980) Krankheits- und Todesursachen beim Igel (Erinaceus europaeus L.) Sektionsfälle 1975 bis 1979. Prakt Tierarzt 9:744–746.
- 22. Barutzki D, Schmid K, Heine J 1984;Untersuchungen über das Vorkommen von Endoparasiten beim Igel. Berl Muench Tierarztl 97:215–218.
- 23. Barutzki D, Laubmeier E, Forstner MJ (1987) Der Endoparasitenbefall wildlebender und in menschlicher Obhut befindlicher Igel mit einem Beitrag zur Therapie. Tierarztl Prax 15:325–331.
- 24. Majeed SK, Morris PA, Cooper JE (1989) Occurrence of the lungworms Capillaria and Crenosoma spp. in British hedgehogs (Erinaceus europaeus). J Comp Pathol 100:27–36.
- 25. Gaglio G, Allen S, Bowden L, Bryant M, Morgan ER 2010;Parasites of European hedgehogs (Erinaceus europaeus) in Britain: epidemiological study and coprological test evaluation. Eur J Wildlife Res 56:839–844.
- 26. Smales LR, Skuballa J, Taraschewski H, Petney T, Pfäffle M (2010) An immature polymorphid acanthocephalan from a European hedgehog (Erinaceidae) from New Zealand. New Zeal J Zool 37:185–188.
- 27. Haigh A, O'Keeffe J, O'Riordan R, Butler F (2013) A preliminary investigation into the endoparasite load of the European hedgehog (Erinaceus europaeus) in Ireland. Mammalia 78:103–107.
- 28. Cirak VY, Senlik B, Aydogdu A, Selver M, Akyol V (2010) Helminth parasites found in hedgehogs (Erinaceus concolor) from Turkey. Prev Vet Med 97:64–66.
- 29. Mizgajska-Wiktor H, Jarosz W, Pilacinska B, Dziemian S (2010) Helminths of hedgehogs, Erinaceus europaeus and E. roumanicus from Poznan region, Poland – coprological study. Wiad Parazytol 56:329–332.
- 30. Furmaga F (1961) Materials to the helminth fauna of hedgehogs Erinaceus roumanicus Barrett-Hamilton. Acta Parasit 9:441–445.
- 31. Boag B, Fowler PA (1988) The prevalence of helminth parasites from the hedgehog Erinaceus europaeus in Great Britain. J Zool 215:379–382.
- 32. Skuballa J, Taraschewski H, Petney TN, Pfäffle M, Smales LR (2010) The avian acanthocephalan Plagiorhynchus cylindraceus (Palaeacanthocephala) parasitizing the European hedgehog (Erinaceus europaeus) in Europe and New Zealand. Parasitol Res 106:431–437.
- 33. Egli R (2004) Comparison of physical condition and parasite burdens in rural, suburban and urban hedgehogs Erinaceus europaeus: implications for conservation. Diploma thesis, University of Bern.
- 34. Visser M, Rehbein S, Wiedemann C (2001) Species of flea (Siphonaptera) infesting pets and hedgehogs in Germany. J Vet Med 48:192–202.
- 35. Földvari G, Rigo K, Jablonszky M, Biro N, Majoros G, et al. (2011) Ticks and the city: ectoparasites of the northern white-breasted hedgehog (Erinaceus roumanicus) in an urban park. Ticks Tick Borne Dis 2:231–234.
- 36. Beck W, Clark HH (1997) Differentialdiagnose medizinisch relevanter Flohspezies und ihre Bedeutung in der Dermatologie. Hautarzt 48:714–719.
- 37. Beck W, Saunders M, Schunack B, Pfister K (2005) Flohbekämpfung bei wildlebenden und in menschlicher Obhut gepflegten Igeln - ein Therapieansatz mit Nitenpyram (Capstar). Prakt Tierarzt 86:798–802.
- 38. Pfäffle M, Petney T, Skuballa J, Taraschewski H (2011) Comparative population dynamics of a generalist (Ixodes ricinus) and specialist tick (I. hexagonus) species from European hedgehogs. Exp Appl Acarol 54:151–164.
- 39. Beck W (2007) Endoparasiten beim Igel. Wien Klein Wochenschr 119:40–44.
- 40. Feliu C, Blasco S, Torres J, Miquel J, Casanova JC (2001) On the helminthfauna of Erinaceus europaeus Linnaeus, 1758 (Insectivora, Erinaceidae) in the Iberian Peninsula. Res Rev Parasitol 61:31–37.
- 41. Liesegang A, Lehmann MC (2003) Häufigkeit von Krankheit und Abgangsursachen bei Igeln. Schweiz Arch Tierheilkd 145:589–591.
- 42. Saupe E (1988) Die Parasitosen des Igels und ihre Behandlung. Prakt Tierarzt 12:49–54.
- 43. Edelenyi B, Szabo I (1963) Parasitische Würmer in einheimischen Säugetieren. Annls Hist-Nat Mus Nat Hung 55:275–283.
- 44. Prokopic J (1957) Results of the helminthological investigation of hedgehogs in CSR (in Czech). Acta Soc Zool Bohemoslov 21:97–111.
- 45. Dimelow EJ (1963) Observations on the feeding of the hedgehog (Erinaceus europaeus L.). Proc Zool Soc Lond 141:291–309.
- 46. Schütze HR (1980) Nachweis, Entwicklung und Behandlung wichtiger Parasiten des Igels (Erinaceus europaeus L.). Prakt Tierarzt 61:142–146.
- 47. Krehmer E (1967) Starker Befall mit Brachylaemus erinacei (Trematoda: Brachylaemidae) als Todesursache eines Igels. Tieraerztl Umsch 22:524–526.
- 48. Carlson A (1980) Diagnose und Therapie der Parasitosen der Igel. Prakt Tierarzt 62:73–75.
- 49. Schmidt A (1972) On the mechanism of photosynthetic sulfate reduction. Arch Mikrobiol 84:77–86.
- 50. Giannetto S, Niutta PP, Giudice E (1993) Parasitological research on the hedgehog (Erinaceus europaeus) in Sicily. Pest Anim 47:1433–1436.
- 51. Poglayen G, Giannetto S, Scala A, Garippa G, Capelli G, et al. (2003) Helminths found in hedgehogs (Erinaceus europaeus) in three areas of Italy. Vet Rec 4:22–24.
- 52. Kutzer E (1992) Parasitosen von Hund und Katze: Arthropoden. In:Eckert J, Kutzer E, Rommel M, Bürger H-J, Körting Weditors.Veterinärmedizinische Parasitologie. 4th Edition.Hamburg: Verlag Paul Parey. pp.629–645.
- 53. Alvarez F, Iglesias R, Bos J, Rey J, Sanmartin Durán ML (1991) Lung and hearth nematodes in some Spanish mammals. Wiad Parazytol 37:481–490.
- 54. Scala A, Garippa G (1996) Principal helminthiases of the hedgehog (Erinaceus europaeus) in Sardinia: epidemiological anatomical and histopathological findings. In:Spagnesi M, Guberti V, De Marco MAeditors.Atti del Convegno Nazionale: Ecopatologia della Fauna Selvatica, Bologna, Italy, 15–17 dicembre 1994, pp. 151–166.
- 55. Shilova-Krassova SA (1952) On the feeding habits of the hedgehog (Erinaceus europaeus L.) in the southern forests. Zool Zh 31:944–50.
- 56. Brockie RE (1959) Observations of the food of the hedgehog (Erinaceus europaeus L.) in New Zealand. N Z J Sci 2:121–136.
- 57. Kruuk H (1964) Predators and anti-predator behaviour of the black-headed gull (Larus ridibundus L.). Leiden: E.J. Brill.
- 58. Campbell PA (1973) The feeding behaviour of the hedgehog (Erinaceus europaeus L.) in pasture land in New Zealand. N Z J Ecol 20:35–40.
- 59. Yalden DW (1976) The food of the hedgehog in England. Acta Theriol 21:401–424.
- 60. Obrtel R, Holišová V (1981) The diet of hedgehogs in an urban environment. Folia Zool 30:193–201.
- 61. Grosshans W (1983) Zur Nahrung des Igels (Erinaceus europaeus L. 1758). Untersuchungen von Magen-Darminhalten schleswig-holsteinischer Igel. Zool Anz 211:364–384.
- 62. Burgisser H (1983) Compte-rendu sur les maladies des animaux sauvages de 1975 à 1982. Schw Arch Tierheilkd 125:519–527.
- 63. Laubmeier E (1985) Untersuchungen über die Endoparasiten des Igels (Erinaceus europaeus) bei freilebenden und in menschlicher Obhut überwinternden Tieren sowie Entwurmungsversuche mit Ivermectin. Thesis, University of Munich.
- 64. Laux A (1987) Extensität und Intensität des Endoparasitenbefalls beim Igel. Angew Parasitol 28:137–141.
- 65. Döpke C. (2002) Kasuistische Auswertung der Untersuchungen von Igeln (Erinaceus europaeus) im Einsendungsmaterial des Instituts für Pathologie von 1980–2001, DVM thesis, Tierärztliche Hochschule Hannover.
- 66. Pantchev N, Globokar-Vrhovec M, Beck W (2005) Endoparasitosen bei Kleinsäugern aus privater Haltung und Igeln. Labordiagnostische Befunde der koprologischen, serologischen und Urinuntersuchung (2002–2004). Tieraerztl Prax 33:296–306.
- 67. Ribas A, Filipucci MG, Casanova JC (2003) Parasitic helminthes of small mammals in Elba island. Hystrix – It J Mammal 90:793–796.